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Commensal and pathogenic biofilms differently modulate peri-implant oral mucosa in an organotypic model.

ABSTRACT: The impact of oral commensal and pathogenic bacteria on peri-implant mucosa is not well understood, despite the high prevalence of peri-implant infections. Hence, we investigated responses of the peri-implant mucosa to Streptococcus oralis or Aggregatibacter actinomycetemcomitans biofilms using a novel in vitro peri-implant mucosa-biofilm model. Our 3D model combined three components, organotypic oral mucosa, implant material, and oral biofilm, with structural assembly close to native situation. S. oralis induced a protective stress response in the peri-implant mucosa through upregulation of heat shock protein (HSP70) genes. Attenuated inflammatory response was indicated by reduced cytokine levels of interleukin-6 (IL-6), interleukin-8 (CXCL8), and monocyte chemoattractant protein-1 (CCL2). The inflammatory balance was preserved through increased levels of tumor necrosis factor-alpha (TNF-?). A. actinomycetemcomitans induced downregulation of genes important for cell survival and host inflammatory response. The reduced cytokine levels of chemokine ligand 1 (CXCL1), CXCL8, and CCL2 also indicated a diminished inflammatory response. The induced immune balance by S. oralis may support oral health, whereas the reduced inflammatory response to A. actinomycetemcomitans may provide colonisation advantage and facilitate later tissue invasion. The comprehensive characterisation of peri-implant mucosa-biofilm interactions using our 3D model can provide new knowledge to improve strategies for prevention and therapy of peri-implant disease.

SUBMITTER: Ingendoh-Tsakmakidis A

PROVIDER: S-EPMC6771885 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Commensal and pathogenic biofilms differently modulate peri-implant oral mucosa in an organotypic model.

Ingendoh-Tsakmakidis Alexandra A Mikolai Carina C Winkel Andreas A Szafrański Szymon P SP Falk Christine S CS Rossi Angela A Walles Heike H Stiesch Meike M

Cellular microbiology 20190717 10

The impact of oral commensal and pathogenic bacteria on peri-implant mucosa is not well understood, despite the high prevalence of peri-implant infections. Hence, we investigated responses of the peri-implant mucosa to Streptococcus oralis or Aggregatibacter actinomycetemcomitans biofilms using a novel in vitro peri-implant mucosa-biofilm model. Our 3D model combined three components, organotypic oral mucosa, implant material, and oral biofilm, with structural assembly close to native situation. ...[more]

PMID: 31270923

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Project description:Oral health is associated with a symbiotic microbial community and host-microbe homeostasis is maintained by the controlled immune response. Various factors can disrupt this homeostasis. Dysbiosis, which is characterized by increased immune response and a shift in the microbiome, contributes the pathogenesis of peri-implantitis. Peri-implant mucosa and commensal bacteria play important roles in the maintenance of host-microbe homeostasis, but little is known about how they interact. We have therefore investigated the early host-microbe interaction between a commensal multispecies biofilm (Streptococcus oralis, Actinomyces naeslundii, Veillonella dispar, Porphyromonas gingivalis) and peri-implant mucosa at 24 and 48 h. Our in vitro peri-implant mucosa-biofilm model contained organotypic oral mucosa, implant material and biofilm. After 24 h, the biofilm induced a modest innate immune response in the peri-implant mucosa by the upregulation of 5 genes related to immune and inflammatory response and the increased secretion of IL-6 and CCL20. This controlled immune response protected tissue integrity and the peri-implant mucosa remained intact. The secreted antibacterial proteins human β-Defensins-1, -2, and CCL20 controlled the overgrowth of the biofilm by reducing its volume - without affecting the live/dead ratio or bacterial distribution. Thus, host-microbe homeostasis was established within the first 24 h. In contrast, host-microbe homeostasis was disrupted after 48 h. The mucosa was damaged and detached from the implant, due to the induced downregulation of cell adhesion related genes. The immune response was enhanced by upregulation of additional genes related to the immune and inflammatory response and increased secretion of IL-1β, TNF-α, and CCL20. Moreover, bacterial distribution was altered, with an increased proportion of V. dispar. The disrupted host-microbe homeostasis could lead to incipient dysbiosis. This deeper understanding of the early host-microbe interaction at the peri-implant site may provide the basis for new strategies to improve the prevention and therapy of peri-implant diseases.

Dataset Information

Commensal and pathogenic biofilms differently modulate peri-implant oral mucosa in an organotypic model.

Publications

Commensal and pathogenic biofilms differently modulate peri-implant oral mucosa in an organotypic model.

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